It is proposed to investigative, using experiments and computer simulations, the unassisted permeation of short peptides through phospholipid membranes. Peptide Passive Translocations (PPT) are relevant to key questions in biology: (i) PPT suggest transport mechanisms into and out of primordial cells; (ii) PPT participate in insertion of transmembrane helices and membrane machinery; and (iii) PPT are models for the design of efficient permeants for molecular delivery. Studying kinetics and thermodynamics of peptide-membrane processes using atomically detailed physics- based approaches will provide unprecedented insight into permeation and insertion events and to the way biological systems control concentrations gradients and transport. In particular the present study may provide useful guidelines for the design of efficient molecular permeants. However, these investigations are challenging since they are impacted by (i) subtle variations in properties of the membranes and permeants, requiring high accuracy; by (ii) interactions at length scales significantly larger than the permeant dimension requiring large scale simulations; and by (iii) exceptionally broad temporal scales from nanoseconds to hours. Novel experiments and theories will address these challenges. Experimental permeation rates are determined by time- resolved absorption and fluorescence spectroscopy of tryptophan and FRET using chromophores placed strategically throughout the membrane-peptide system. Molecular Dynamics (MD) and Milestoning simulations of these systems, which closely mimic biological environments, will be conducted. We start our joint experimental-theoretical collaboration with a transmembrane helix, and continue to investigate the permeation of a single amino acid through a pure DMPC or DOPC membrane. We end with peptides crossing a membrane enriched with transmembrane helices, cholesterol (chol) or 6- ketocholestanol (6ket) molecules. The last system mimics true biological environments.